Patterns and processes of genome-wide divergence between North American and African Drosophila melanogaster

Genetics

Volumn 186, Issue 1, 2010, Pages 219-239

  Yukilevich, Roman ^a   Turner, Thomas L ^b   Aoki, Fumio ^c   Nuzhdin, Sergey V ^d   True, John R ^c  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^d STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; AUTOSOME; CAMEROON; CENTRAL AMERICA; CENTROMERE; DEMOGRAPHY; DROSOPHILA MELANOGASTER; FEMALE; GENE FREQUENCY; GENE SEQUENCE; GENETIC VARIABILITY; GEOGRAPHIC DISTRIBUTION; HAPLOTYPE; INSECT GENOME; MALE; NONHUMAN; NORTH AFRICA; NORTH AMERICA; POPULATION DISPERSAL; PRIORITY JOURNAL; UNITED STATES; X CHROMOSOME; ZIMBABWE;

AFRICA; ANALYSIS OF VARIANCE; ANIMALS; DROSOPHILA MELANOGASTER; FEMALE; GENETIC VARIATION; GENOME, INSECT; GENOMICS; MALE; NORTH AMERICA; SEQUENCE ANALYSIS, DNA;

DROSOPHILA MELANOGASTER;

EID: 78751667441     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.110.117366     Document Type: Article

References (90)

1. ACHERE, V., J. M. FAVRE, G. BESNARD and S. JEANDROZ, 2005 Genomic organization of molecular differentiation in Norway spruce (Picea abies). Mol. Ecol. 14: 3191-3201. (Pubitemid 43919358)
2. AGUADE, M., 2009 Nucleotide and copy-number polymorphism at the odorant receptor genes Or22a and Or22b in Drosophila melanogaster. Mol. Biol. Evol. 26: 61-70.
3. AGUADE, M., N. MIYASHITA and C. H. LANGLEY, 1989 Reduced variation in the yellow-achaete-scute region in natural populations of Drosophila melanogaster. Genetics 122: 607-615.
4. ANDOLFATTO, P., 2001 Contrasting patterns of X-linked and autosomal nucleotide variation in Drosophila melanogaster and Drosophila simulans. Mol. Biol. Evol. 18: 279-290.
5. BAUDRY, E., B. VIGINIER and M. VEUILLE, 2004 Non-African populations of Drosophila melanogaster have a unique origin. Mol. Biol. Evol. 21: 1482-1491.
6. BEAUMONT, M. A., and D. J. BALDING, 2004 Identifying adaptive genetic divergence among populations from genome scans. Mol. Ecol. 13: 969-980.
7. BEGUN, D. J., and C. F. AQUADRO, 1993 African and North American populations of Drosophila melanogaster are very different at the DNA level. Nature 365: 548-550.
8. BEGUN, D. J., and C. F. AQUADRO, 1995 Evolution at the tip and base of the X chromosome in an African population of Drosophila melanogaster. Mol. Biol. Evol. 12(3): 382-390.
9. BEGUN, D. J., A. K. HOLLOWAY, K. STEVENS, L. W. HILLIER, Y. P. POH et al., 2007 Population genomics: whole genome analysis of polymorphism and divergence in Drosophila simulans. PLoS Biol. 5(11): e310.
10. BENJAMINI, Y., and Y. HOCHBERG, 1995 Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Statist. Soc. B 57: 289-300.
11. BENJAMINI, Y., and D. YEKUTIELI, 2001 The control of false discovery rate under dependency. Ann. Stat. 29: 1165-1188.
12. BONIN, A., P. TABERLET, C. MIAUD and F. POMPANON, 2006 Explorative genome scan to detect candidate loci for adaptation along a gradient of altitude in the common frog (Rana temporaria). Mol. Biol. Evol. 23: 773-783.
13. BONIN, A., D. EHRICH and S. MANEL, 2007 Statistical analysis of amplified fragment length 30 polymorphism data: a toolbox for molecular ecologists and evolutionist. Mol. Ecol. 16: 3737-3758.
14. BOREVITZ, J. O., D. LIANG, D. PLOUFFE, H. S. CHANG, T. ZHU et al., 2003 Large scale identification of single feature polymorphisms in complex genomes. Genome Res. 13: 513-523.
15. CAMPBELL, D., and L. BERNATCHEZ, 2004 Generic scan using AFLP markers as a means to assess the role of directional selection in the divergence of sympatric whitefish ecotypes. Mol. Biol. Evol. 21: 945-956.
16. CAPY, P., E. PLA and J. R. DAVID, 1994 Phenotypic and genetic variability of morphometrical traits in natural populations of D. melanogaster and D. simulans. II. Genet. Sel. Evol. 26: 15-28.
17. CARACRISTI, G., and C. SCHLÖTTERER, 2003 Genetic differentiation between American and European D. melanogaster populations could be attributed to African alleles. Mol. Biol. Evol. 20: 792-799.
18. CHARLESWORTH, B., 1998 Measures of divergence between populations and the effect of forces that reduce variability. Mol. Biol. Evol. 15(5): 538-543.
19. CHARLESWORTH, B., 2001 The effect of life-history and mode of inheritance on neutral genetic variability. Genet. Res. 77: 153-166.
20. CHARLESWORTH, B., J. A. COYNE and N. H. BARTON, 1987 The relative rates of evolution of sex chromosomes and autosomes. Am. Nat. 130: 113-146.
21. COLEGRAVE, N., H. HOLLOCHER, K. HINTON and M. G. RITCHIE, 2000 The courtship song of African Drosophila melanogaster. J. Evol. Biol. 13: 143-150.
22. DAVID, J. R., and P. CAPY, 1988 Genetic variation of Drosophila melanogaster natural populations. Trends Genet. 4(4): 106-111.
23. DE HOON, M. J. L., S. IMOTO, J. NOLAN and S. MIYANO, 2004 Open Source Clustering Software. Bioinformatics 20(9): 1453-1454.
24. DOPMAN, E., B., and D. L. HARTL. 2007 A portrait of copy-number polymorphism in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 104(50): 19920-19925.
25. EMELIANOV, I., F. MAREC and J.MALLET, 2003 Genomic evidence for divergence with gene flow in host races of the larch budmoth. Proc. R. Soc. Lond. B 271: 97-105.
26. EMERSON, J. J., M. CARDOSO-MOREIRA, J. O. BOREVITZ and M. LONG, 2008 Natural selection shapes genome-wide patterns of copy-number polymorphism in Drosophila melanogaster. Science 320: 1629-1631.
27. FAY, J. C., and C. I. WU, 2000 Hitchhiking under positive Darwinian selection. Genetics 155: 1405-1413.
28. FELSENSTEIN, J., 2004 PHYLIP (Phylogeny Inference Package), Version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle.
29. FORD, M. J., and C. F. AQUADRO, 1996 Selection on X-linked genes during speciation in the Drosophila athabasca complex. Genetics 144: 689-703.
30. GAUTIER, L., L. COPE, B.M. BOLSTAD and R. A. IRIZARRY, 2004 affy: analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20: 307-315.
31. GLINKA, S., L. OMETTO, S.MOUSSET, W. STEPHAN and D. DE LORENZO, 2003 Demography and natural selection have shaped genetic variation in Drosophila melanogaster: a multi-locus approach. Genetics 165: 1269-1278.
32. GRESHAM, D., D. RUDERFER, S. PRATT, J. SCHACHERER, M. DUNHAM et al., 2006 Genome-wide detection of polymorphisms at nucleotide resolution with a single DNA microarray. Science 311(5769): 1932-1936.
33. HADDRILL, P. R., K. R. THORNTON, B. CHARLESWORTH and P. ANDOLFATTO, 2005 Multilocus patterns of nucleotide variability and the demographic and selection history of Drosophila melanogaster populations. Genome Res. 15: 790-799.
34. HAHN, M. W., 2008 Toward a selection theory of molecular evolution. Evolution 62: 255-265.
35. HAMBLIN, M. T., A. M. CASA, H. SUN, S. C. MURRAY, A. H. PATERSON et al., 2006 Challenges of detecting directional selection after a bottleneck: lessons from Sorghum bicolor. Genetics 173: 953-964.
36. HOLLOCHER, H., C.-T. TING, F. POLLACK and C. I. WU, 1997 Incipient speciation by sexual isolation in Drosophila melanogaster: variation in mating preference and correlation between sexes. Evolution 51(4): 1175-1181.
37. HUDSON, R. R., 2002 Generating samples under a Wright-Fisher neutral model of genetic variation. Bioinformatics 18: 337-338.
38. HUTTER, S., H. LI, S. BEISSWANGER, D. DE LORENZO and W. STEPHAN, 2007 Distinctly different sex ratios in African and European populations of Drosophila melanogaster inferred from chromosomewide single nucleotide polymorphism data. Genetics 177: 469-480.
39. KAUER, M. O., B. ZANGERL, D. DIERINGER and C. SCHLÖTTERER, 2002 Chromosomal patterns of microsatellite variability contrast sharply in African and non-African populations of Drosophila melanogaster. Genetics 160: 247-256.
40. KAUER, M. O., D. DIERINGER and C. SCHLÖTTERER, 2003 A microsatellite variability screen for positive selection associated with the "out of Africa" habitat expansion of Drosophila melanogaster. Genetics. 165: 1137-1148.
41. KELLER, A., 2007 Drosophila melanogaster's history as a human commensal. Curr. Biol. 17(3): R77-R81.
42. KULATHINAL, R. J., S. M. BENNETT, C. L. FITZPATRICK and M. A. NOOR, 2008 Fine-scale mapping of recombination rate in Drosophila refines its correlation to diversity and divergence. Proc. Natl. Acad. Sci. USA 105: 10051-10056.
43. KULATHINAL, R. J., L. S. STEVISON and M. A. F. NOOR, 2009 The genomics of speciation in Drosophila: diversity, divergence and introgression on a genome-wide scale. PLoS Genet. 5: e1000550.
44. LANGLEY, C. H., J. MACDONALD, N. MIYASHITA and M. AGUADD, 1993 Lack of correlation between interspecific divergence and intraspecific polymorphism at the suppressor of forked region in Drosophila melanogaster and Drosophila simulans. Proc. Natl. Acad. Sci. USA 90: 1800-1803.
45. MACPHERSON, J. M., J. GONZALEZ, D. WITTEN, J. C. DAVIS, N. ROSENBERG et al., 2008 Nonadaptive explanations for signatures of partial selective sweeps in Drosophila. Mol. Biol. Evol. 25(6): 1025-1042.
46. MAYNARD SMITH, J., and J. HAIGH, 1974 The hitch-hiking effect of a favourable gene. Genet. Res. 23: 23-35.
47. MURRAY, M. C., and M. P. HARE, 2006 A genomic scan for divergent selection in a secondary contact zone between Atlantic and Gulf of Mexico oysters, Crassostrea virginica. Mol. Ecol. 15: 4229-4242.
48. NEI, M., 1987 Molecular Evolutionary Genetics. Columbia University Press, New York.
49. NOOR, M. A. F., and S. M. BENNETT, 2009 Islands of speciation or mirages in the desert? Examining the role of restricted recombination in maintaining species. Heredity 103(6): 439-444.
50. NOOR, M. A. F., and J. L. FEDER, 2006 Speciation genetics: evolving approaches. Nat. Rev. Genet. 7: 851-861.
51. NOSIL, P., S. P. EGAN and D. J. FUNK, 2008 Heterogeneous genomic differentiation between walking-stick ecotypes: 'isolation by adaptation' and multiple roles for divergent selection. Evolution 62: 316-336.
52. NOSIL, P., D. J. FUNK and D. ORTIZ-BARRIENTOS, 2009 Heterogenous genomic divergence during speciation. Mol. Ecol. 18(3): 375-402.
53. OMETTO, L., S. GLINKA, D. DE LORENZO and W. STEPHAN, 2005 Inferring the effects of demography and selection on Drosophila melanogaster populations from a chromosome-wide scan of DNA variation. Mol. Biol. Evol. 22: 2119-2130.
54. ORR, H. A., and A. J. BETANCOURT, 2001 Haldane's sieve and adaptation from the standing genetic variation. Genetics 157: 875-884.
55. POOL, J. E., and C. F. AQUADRO, 2006 History and structure of sub-Saharan populations of Drosophila melanogaster. Genetics 174: 915-929.
56. PRZEWORSKI, M., 2002 The signature of positive selection at randomly chosen loci. Genetics 160: 1179-1189.
57. ROSENBERG, M. S., 2004 PASSAGE. Pattern Analysis, Spatial Statistics, and Geographic Exegesis, Version 1.0. Department of Biology, Arizona State University, Tempe, AZ.
58. ROUAULT, J., P. CAPY and J. M. JALLON, 2001 Variations of male cuticular hydrocarbons with geoclimatic variables: An adaptative mechanism in Drosophila melanogaster? Genetica 110: 117-130.
59. ROZAS, J., J. C. SANCHEZ-DELBARRIO, X. MESSEGUER and R. ROZAS, 2003 DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19: 2496-2497.
60. SAVOLAINEN, V., M. C. ANSTETT, C. LEXER, I. HUTTON, J. J. CLARKSON et al., 2006 Sympatric speciation in palms on an oceanic island. Nature 441: 210-213.
61. SCHMIDT, P. S., C. T. ZHU, J. DAS, M. BATAVIA, L. YANG et al., 2008 An amino acid polymorphism in the couch potato gene forms the basis for climatic adaptation in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 105: 16207-16211.
62. SCHÖFL, G., and C. SCHLÖTTERER, 2004 Patterns of microsatellite variability among X chromosomes and autosomes indicate a high frequency of beneficial mutations in non-African D. simulans. Mol. Biol. Evol. 21(7): 1384-1390.
63. SCHÖFL, G., F. CATANIA, V. NOLTE and C. SCHLÖTTERER, 2005 African sequence variation accounts for most of the sequence polymorphism in non-African Drosophila melanogaster. Genetics 170: 1701-1709.
64. SCOTTI-SAINTAGNE, C., S. MARIETTE, I. PORTH, P. G. GOICOECHEA, T. BARRENECHE et al., 2004 Genome scanning for interspecific differentiation between two closely related oak species. [Quercus robur L. and Q. petraea (Matt.) Liebl.] Genetics 168: 1615-1626.
65. SELLA, G., D. A. PETROV, M. PRZEWORSKI and P. ANDOLFATTO, 2009 Pervasive natural selection in the Drosophila genome? PLoS Genet. 5(6): e1000495.
66. SEZGIN, E., D. D. DUVERNELL, L. M. MATZKIN, Y. DUAN, C.-T. ZHU et al., 2004 Single-locus latitudinal clines and their relationship to temperate adaptation in metabolic genes and derived alleles in Drosophila melanogaster. Genetics 168: 923-931.
67. SHAPIRO, J. A., W. HUANG, C. ZHANG, M. J. HUBISZ, J. LU et al., 2007 Adaptive genic evolution in the Drosophila genomes. Proc. Natl. Acad. Sci. USA 104: 2271-2276.
68. SINGH, N. D., J. M. MACPHERSON, J. D. JENSEN and D. A. PETROV, 2007 Similar levels of X-linked and autosomal nucleotide variation in African and non-African populations of Drosophila melanogaster. BMC Evol. Biol. 7: 202.
69. STEPHAN, W., and H. LI, 2007 The recent demographic and adaptive history of Drosophila melanogaster. Heredity 98: 65-68. (Pubitemid 46173894)
70. STINCHCOMBE, J. R., and H. E. HOEKSTRA, 2008 Combining population genomics and quantitative genetics: finding the genes underlying ecologically important traits. Heredity 100: 158-170.
71. STOREY, J.D., and R. Tibshirani, 2003 Statistical significance for genome-wide studies. Proc. Natl. Acad. Sci. USA 100: 9440-9445.
72. TAJIMA, F., 1989 Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585-595.
73. TAKAHASHI, A., S. C. TSAUR, J. A. COYNE and C. I. WU, 2001 The nucleotide changes governing cuticular hydrocarbon variation and their evolution in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 98: 3920-3925.
74. THORNTON, K. R., and P. ANDOLFATTO, 2006 Approximate Bayesian inference reveals evidence for a recent, severe bottleneck in a Netherlands population of Drosophila melanogaster. Genetics 172: 1607-1619.
75. TURNER, T. L., M. W. HAHN and S. V. NUZHDIN, 2005 Genomic islands of speciation in Anopheles gambiae. PloS Biol. 3(9): 1572-1574.
76. TURNER, T. L., M. T. LEVINE and D. J. BEGUN, 2008a Genomic analysis of adaptive differentiation in Drosophila melanogaster. Genetics 179: 455-473.
77. TURNER, T. L., E. J. WETTBERG and S. V. NUZHDIN, 2008b Genomic analysis of differentiation between soil types reveals candidate genes for local adaptation in Arabidopsis lyrata. PLoS ONE 3(9): e3183.
78. VASEMAGI, A., J. NILSSON and C. R. PRIMMER, 2005 Expressed sequence taglinked microsatellites as a source of gene-associated polymorphisms for detecting signatures of divergent selection in Atlantic salmon (Salmo salar L.). Mol. Biol. Evol. 22: 1067-1076.
79. VICOSO, B., and B. CHARLESWORTH, 2006 Evolution on the X chromosome: unusual patterns and processes. Nat. Rev. Genet. 7: 645-653.
80. VICOSO, B., and B. CHARLESWORTH, 2009 Effective population size and the faster-X effect: an extended model. Evolution 63(9): 2413-2426.
81. WALL, J. D., P. ANDOLFATTO and M. PRZEWORSKI, 2002 Testing models of selection and demography in Drosophila simulans. Genetics 162: 203-216.
82. WEIR, B. S., and C. C. COCKERHAM, 1984 Estimating F-statistics for the analysis of population structure. Evolution 38: 1358-1370.
83. WILDING, C. S., R. K. BUTLIN and J. GRAHAME, 2001 Differential gene exchange between parapatric morphs of Littorina saxatilis detected using AFLP markers. J. Evol. Biol. 14: 611-619.
84. WINZELER, E. A., D. R. RICHARDS, A. R. CONWAY, A. L. GOLDSTEIN, S. KALMAN et al., 1998 Direct allelic variation scanning of the yeast genome. Science 281: 1194-1197.
85. WU, C-I., H. HOLLOCHER, D. J. BEGUN, C. F. AQUADRO, Y. XU et al., 1995 Sexual isolation in Drosophila melanogaster: a possible case of incipient speciation. Proc. Natl. Acad. Sci. USA 92: 2519-2523.
86. YATABE, Y., N. C. KANE, C. SCOTTI-SAINTAGNE and L. H. RIESEBERG, 2007 Rampant gene exchange across a strong reproductive barrier between the annual sunflowers, Helianthus annuus and H. petiolaris. Genetics 175: 1883-1893.
87. YUKILEVICH, R., and J. R. TRUE, 2008a Incipient sexual isolation among cosmopolitan Drosophila melanogaster populations. Evolution 62(8): 2112-2121.
88. YUKILEVICH, R., and J. R. TRUE, 2008b African morphology, behavior and pheromones underlie incipient sexual isolation between US and Caribbean Drosophila melanogaster. Evolution 62(11): 2807-2828.
89. ZENG, K., Y.-X. FU, S. SHI and C.-I. WU, 2006 Statistical tests for detecting positive selection by utilizing high-frequency variants. Genetics 174: 1431-1439.
90. ZHANG, L., M. F. MILES and K. D. ALDAPE, 2003 A model of molecular interactions on short oligonucleotide microarrays. Nat. Biotechnol. 21(7): 818-821.